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Original article
Inattention in very preterm children: implications for screening and detection
  1. Ellen Brogan1,
  2. Lucy Cragg2,
  3. Camilla Gilmore3,
  4. Neil Marlow4,
  5. Victoria Simms5,6,
  6. Samantha Johnson5
  1. 1Leicester Children's Hospital, University Hospitals of Leicester NHS Trust, Leicester, UK
  2. 2School of Psychology, University of Nottingham, Nottingham, UK
  3. 3Mathematics Education Centre, Loughborough University, Loughborough, UK
  4. 4Research Department of Academic Neonatology, Institute for Women's Health, University College London, London, UK
  5. 5Department of Health Sciences, University of Leicester, Leicester, UK
  6. 6School of Psychology, University of Ulster, Coleraine, UK
  1. Correspondence to Dr Samantha Johnson, Department of Health Sciences, University of Leicester, 22–28 Princess Road West, Leicester, LE1 6TP, UK; sjj19{at}le.ac.uk

Abstract

Objective Children born very preterm (VP; <32 weeks) are at risk for attention deficit/hyperactivity disorders (ADHD). ADHD in VP children have a different clinical presentation to ADHD in the general population, and therefore VP children with difficulties may not come to the teacher's attention in school. We have assessed ADHD symptoms to determine whether VP children's difficulties may go undetected in the classroom.

Design Parents and teachers of 117 VP and 77 term-born children completed the Strengths and Difficulties Questionnaire to assess hyperactivity/inattention, emotional, conduct and peer problems, and the Du Paul ADHD Rating Scale-IV to assess inattention and hyperactivity/impulsivity symptoms. Special Educational Needs (SEN) were assessed using teacher report. Group differences in outcomes were adjusted for socio-economic deprivation.

Results Parents and teachers rated VP children with significantly higher mean Strengths and Difficulties Questionnaire hyperactivity/inattention scores, and parents rated them with more clinically significant hyperactivity/inattention difficulties than term-born controls (Relative Risk (RR) 4.0; 95% CI 1.4 to 11.4). Examining ADHD dimensions, parents and teachers rated VP children with significantly more inattention symptoms than controls, and parents rated them with more clinically significant inattention (RR 4.8; 95% CI 1.4 to 16.0); in contrast, there was no excess of hyperactivity/impulsivity. After excluding children with SEN, VP children still had significantly higher inattention scores than controls but there was no excess of hyperactivity/impulsivity.

Conclusions VP children are at greater risk for symptoms of inattention than hyperactivity/impulsivity. Inattention was significantly increased among VP children without identified SEN suggesting that these problems may be difficult to detect in school. Raising teachers’ awareness of inattention problems may be advantageous in enabling them to identify VP children who may benefit from intervention.

  • Child Psychology
  • General Paediatrics
  • Neonatology
  • Neurodevelopment
  • Psychology

https://doi.org/10.1136/archdischild-2013-305532

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    What is already known on this topic?

    • Children born very preterm are at increased risk for psychiatric disorders, especially attention deficit/hyperactivity disorders (ADHD).

    • It has been suggested that inattention is a core deficit among very preterm children with ADHD symptoms.

    • Inattention is a key predictor of poor performance at school.

    What this study adds?

    • Very preterm children's ADHD symptoms are underscored by a core deficit in inattention.

    • Among children without identified special educational needs, very preterm children had significantly higher levels of inattention than their term-born classmates.

    • Raising teachers’ awareness of inattention problems may enable them to identify very preterm children who may benefit from educational intervention.

    Very preterm (VP; <32 weeks) birth is associated with an increased risk of a cluster of mental health disorders, namely anxiety disorders, autism spectrum disorders and attention deficit/hyperactivity disorders (ADHD).1 ADHD and attention problems are the most common adverse behavioural outcomes following VP birth.2–6 Even in the absence of diagnoses there is a generally higher level of attention difficulties among children born preterm; this results in a substantial number with symptoms that fall below the diagnostic threshold yet which may impact on daily activities and performance at school.7–9 In particular, a number of studies have reported a higher risk for inattention than hyperactivity/impulsivity, for symptoms and diagnoses,3 ,4 ,7 ,9 ,10 and a lack of comorbid conduct disorders among VP children.2–4 ,6 These findings are suggestive of a core deficit in inattention in preterm populations.

    Behaviour problems are associated with poor school performance and inattention in particular is a key predictor of academic attainment.9 It is thus unsurprising that VP children have poorer academic attainment than term-born peers and an increased prevalence of Special Educational Needs (SEN).11 ,12 The clinical presentation of ADHD associated with preterm birth also has specific implications for the classroom. Given the lack of comorbid conduct disorders, VP children may not come to the teacher's attention as having behavioural difficulites as readily as other children with ADHD who are hyperactive or disruptive in the classroom. While children with hyperactivity/impulsivity may be identified as having SEN, the needs of those with ‘purer’ inattention problems may therefore go undetected in school.

    The aims of this study were to assess the behavioural outcomes of VP children and to explore the relative impact of VP birth on symptoms of inattention versus hyperactivity/impulsivity. We hypothesised that VP children would have significantly higher levels of inattention than hyperactivity/impulsivity and that there would be a significant excess of inattention among VP children who are not identified with SEN.

    Participants and methods

    Participants

    VP children and term-born controls aged 8–10 years were invited to participate in the Premature Infants’ Skills in Mathematics (PRISM) study, a multicentre study of educational and behavioural outcomes following VP birth. All children born VP (<32 weeks) from September 2001 to August 2003 and admitted for neonatal intensive care in two centres (University Hospitals of Leicester and University College London Hospitals, UK) were invited to participate. A term-born control group was also recruited. For each VP child, three classmates closest in age and of the same sex were identified from which one was selected at random using established procedures.12 Controls born <37+0 weeks were excluded and a control child was not recruited where assessments were conducted at home rather than school, resulting in fewer controls than VP children. Most children recruited to the study still lived in London and the East Midlands and all attended mainstream schools in England. Parents and children received a study information sheet and parents provided written consent.

    Measures

    Parents and teachers were asked to complete study questionnaires. Children were in mainstream primary schools and therefore their main class teacher was asked to complete the questionnaire to ensure familiarity with the child's behaviour in the classroom. Both respondents completed the Strengths and Difficulties Questionnaire (SDQ),13 a 25-item questionnaire to screen for behavioural and emotional disorders. The SDQ yields subscale scores (range 0–10) for four problem domains that assess emotional difficulties, conduct problems, peer relationship difficulties and hyperactivity/inattention. An additional 5-item supplement was also used to assess the impact of problems on the child's daily life comprising impact on home life, friendships, learning and leisure activities. Scores for the four problem domains were combined to give a total difficulties score (range 0–40); higher scores indicate greater difficulties. Scores were compared with cut-off scores for classifying children with clinically significant difficulties (abnormal screens) corresponding with scores >90th centile in the standardisation sample.13 ,14

    As SDQ hyperactivity/inattention scores are a composite score reflecting problems on both dimensions, symptoms of inattention and hyperactivity/impulsivity corresponding with ADHD diagnostic criteria were further explored using the Du Paul ADHD Rating Scale-IV,15 completed by parents and teachers. Raw scores were summed for each dimension with higher scores indicating greater difficulties. Age-specific and gender-specific centile scores were also derived using published norms15 from which scores >90th centile were used to identify children with difficulties on each dimension to correspond with SDQ cut-offs.

    Children in England are identified as having SEN if they have a ‘learning difficulty which calls for special educational provision’.16 Information about SEN was obtained using teacher questionnaires. Information obtained via parent report was used to classify mothers’ highest educational qualification and socio-occupational status using the National Statistics Socio-Economic Classification.17 National Statistics Index of Multiple Deprivation (IMD)18 ranks were also derived using current postcode of residence and were used to determine whether each child lived in the least, middle or most deprived areas of England.

    Statistical analyses

    Data were double entered into two IBM SPSS Statistics V.20 databases. These databases were compared and all discrepancies were verified with the original study records to ensure the accuracy of entered data. Study data were then analysed using IBM SPSS Statistics V.20. Between-group differences in continuous variables were analysed using linear regression with effect sizes reported as mean differences with 95% CIs. To assess group differences in the proportion of children with abnormal screens, Poisson regressions with robust CIs were used with effect sizes reported as relative risk (RR) with 95% CI. Given the marginally significant (p=0.06) association of socio-economic deprivation with group membership, all between-group comparisons were adjusted for deprivation using multivariable analyses with IMD tertile entered as a covariate. Unadjusted results are presented in online supplementary appendixes A and B. All p values were two-tailed.

    Results

    Study sample

    Of the whole VP population (n=266), parents of 125 children responded to invitations to participate in the PRISM study. As this study required children to participate in standardised tests of cognitive and educational attainment, 8 children were excluded (2 lived abroad, 3 attended special school and 3 had severe disability precluding them from participating in study tests) and 117 (44%) were recruited. Teacher questionnaires were returned for 98 (84%) children and parent questionnaires for 101 (86%); at least one questionnaire was returned for 112 (95%) children. There were no significant differences between VP children recruited and not recruited in birth weight (mean difference −6 g; 95%CI −105 g to 93 g, p=0.90) or gestational age (−0.2 weeks, −0.1 to 0.3, p=0.50), and there was no association between recruitment and IMD group (χ2=3.62, p=0.16). Thus the sample recruited was representative of the total population in terms of key variables influencing long-term outcomes.

    As described above, one randomly selected classmate for each VP child was invited to participate in the study. In total, 78 control children were recruited, of which one was later excluded due to preterm birth. The full sample thus comprised 77 term-born controls. Teacher questionnaires were returned for 72 (94%) and parent questionnaires for 66 (86%) children; at least one questionnaire was returned for 76 (99%) children. Characteristics of VP children and controls for whom questionnaires were obtained are shown in table 1. Given the marginally significant difference in socio-economic deprivation between the groups, all analyses were adjusted for IMD group.

    View this table:
    Table 1

    Characteristics of children and their mothers who participated in the study

    Prevalence of behaviour problems

    After adjustment for socio-economic deprivation, parents rated VP children with significantly higher mean scores than controls for conduct problems, hyperactivity/inattention and total difficulties. Teachers rated VP children with significantly higher emotional, hyperactivity/inattention problems and total difficulties. Teachers also rated VP children with higher impact scores indicating a greater frequency of problems that affected VP children's daily activities (table 2). Using published cut-offs for identifying children with clinically significant difficulties, parents rated VP children with four times increased risk for hyperactivity/inattention problems, but teacher ratings were not significantly different from controls. There was no statistically significant difference in other domains as rated by parents and teachers, but both respondents rated preterm children with problems that had a significantly greater impact on their daily life (table 2).

    View this table:
    Table 2

    SDQ and ADHD Rating Scale scores for very preterm children and term-born controls adjusted for IMD tertile

    ADHD symptoms

    Parents and teachers rated VP children with significantly higher mean inattention scores than controls with a difference of three points. In contrast, neither parents nor teachers rated VP children with a significant excess of hyperactivity/impulsivity symptoms (table 2; figure 1A). Repeated measures t tests were used to explore the difference in inattention and hyperactivity/impulsivity ratings within both groups. Among VP children, parents (mean difference 2.57, 95% CI 1.77 to 3.37, p<0.001) and teachers (3.91, 2.75 to 5.09, p<0.001) rated them with significantly higher inattention than hyperactivity/impulsivity. In contrast, there was no statistically significant difference in parents’ ratings of inattention versus hyperactivity/impulsivity among control children; teachers reported significantly higher scores for inattention than hyperactivity/impulsivity among controls (0.97, 0.24 to 1.70, p=0.010), but this difference was significantly smaller than for VP children (ie, no overlap in CIs). To further explore interaction effects, difference scores (inattention minus hyperactivity/impulsivity) were calculated for each child for parent and teacher ratings. Using linear regression with difference scores as a dependent variable, group was a significant predictor for parent (p=0.009) and teacher reports (p<0.001), with VP children displaying significantly larger mean difference scores than control children for parent (VP: mean 1.92, SD 3.45; Control: mean 0.40, SD 3.42) and teacher ratings (VP: mean 1.91, SD 3.27; Control: mean 0.36, SD 2.11). Using scores >90th centile, parents rated VP children with almost five times increased risk for clinically significant inattention problems but there was no significant excess of hyperactivity/impulsivity; teachers ratings were not significantly different between groups (table 2).

    Figure 1
    Figure 1

    Mean difference (95% CI) in z-scores for teacher-rated and parent-rated inattention and hyperactivity/impulsivity symptoms between very preterm children and term-born controls adjusted for socio-economic deprivation. (A) shows data for all children. (B) shows data for children without identified special educational needs (SEN). Higher z-scores indicate a higher level of symptoms in each domain.

    Behaviour problems in children without identified SEN

    Overall, 41 (42%) VP children and 13 (18.3%) controls had identified SEN (adjusted RR 2.3, 95% CI 1.3 to 3.9, p=0.003). When children with SEN were excluded from the analyses, parents still rated VP children with significantly higher SDQ conduct problems and hyperactivity/inattention scores than controls, and teachers rated them only with significantly higher hyperactivity/inattention. As children with SEN were excluded, we did not find an excess of clinically significant problems as expected (table 3).

    View this table:
    Table 3

    SDQ and ADHD Rating Scale scores for children without identified special educational needs adjusted for IMD tertile

    ADHD symptoms in children without identified SEN

    After excluding children with SEN, VP children still had significantly higher inattention scores than controls as rated by parents and teachers; in contrast, there was no significant excess of hyperactivity/impulsivity in either parent or teacher ratings (table 3, figure 1B). There was no excess of clinically significant ADHD symptoms once children with SEN were excluded from the analyses.

    Discussion

    This study advances our understanding of the nature of ADHD symptoms among children born VP and provides further evidence that these are associated with a core deficit in inattention. Commensurate with previous studies, ADHD problems were most consistently elevated among VP children.3 ,5 ,19 Although respondents differed in their ratings of emotional symptoms and conduct problems, parents and teachers rated VP children with signficiantly higher hyperactivity/inattention scores than controls; parents also rated them with a fourfold increased risk of clinically significant difficulties in this domain. In terms of risk ratios these results are similar to those of previous studies.1

    The SDQ hyperactivity/inattention scale assesses problems associated with hyperactivity/impulsivity (three items) and inattention (two items). Scores may therefore reflect an excess of symptoms on either dimension, potentially masking differences in the profile of symptoms among clinical populations. Previous studies of extremely preterm children (<26 weeks) or those born with extremely low birth weight have indicated that ADHD among preterm children may be associated with a specific risk for inattention in terms of symptoms and disorders.3 ,4 ,7 ,9 Using a more detailed analysis of ADHD symptoms along separable dimensions we found that VP children had signifcantly higher inattention than hyperactivity/impulsivity scores and, compared with term-born controls, were at increased risk only for inattention symptoms. Our results thus provide further evidence that inattention is a core deficit among this population.

    In addition to these findings, it is becoming increasingly evident that ADHD symptoms and disorders are rarely associated with comorbid conduct disorders among children born VP.4 Thus, unlike children in the general population with ADHD or other externalising behaviours, VP children are less likely to be disruptive in school and may be less likely to come to the teacher's attention as having difficulties. In fact, we have shown that even after excluding children with identified SEN, VP children still had significantly higher SDQ hyperactivity/inattention scores than term-born peers. Scores on the ADHD rating scale showed this increase was specific to inattention rather than hyperactivity/impulsivity.

    Taken together these findings support our hypothesis that VP children with hyperactivity/impulsivity are more readily identified with SEN than those who have only inattention difficulties, and that an excess of inattention may still be present among those not receiving support in the classroom. This may reflect a general tendency for problems associated with preterm birth to go undetected in school. It has been argued that VP children are part of a growing generation of children with complex learning difficulties and disabilities that differ from those of previous generations and for which new approaches to screening and intervention are needed.20 It has been shown that teachers lack knowledge of the cognitive and behavioural outcomes and educational needs of children born preterm and that less than 10% feel they have received sufficient training in this area.21 This lack of knowledge may impact on teachers’ awareness of the types of difficulties that VP children may present with and thus their ability to readily identify those children who have such problems in the classroom. Improving education professionals’ awareness of the special constellation of cognitive and behavioural sequelae following preterm birth may therefore aid them in detecting inattention in the classroom and in providing appropriate support for VP children with these difficulties.

    A significant increase in SDQ scores among VP children without SEN is a notable finding because even 1-point increases in total difficulties scores are associated with an increased risk of psychiatric disorders.22 Moreover, the significant excess of inattention is concerning as this is a key predictor of long-term academic attainment.9 Inattention symptoms have been associated with poor working memory in VP children,23 ,24 and inattention and working memory are important factors influencing academic attainment in preterm and general population samples.9 ,25 ,26 Routine screening for inattention in educational settings may therefore help in targeting the provision of SEN support and in identifying VP children with subtle, subclinical difficulties. The results of this study are thus useful for informing policy for screening and referral in this population.

    In total, parents and teachers rated 21% of VP children with abnormal total difficulties scores and 23–24% of VP children with difficulties that impacted on their daily living. Our results are thus similar to the ∼25% prevalence of psychiatric disorders reported in various preterm populations.1 ,27 Consistent with previous studies,5 ,28 ,29 teachers generally rated children with fewer difficulties than parents. Teachers’ views of children's behaviours may be influenced by the school environment and by a different perspective arising from the observation of greater numbers of children. Given the known effects of report source bias,5 ,30 we solicited ratings from parents and teachers to provide multi-informant data.

    The strengths of this study lie in the recruitment of a sample of VP children who were representative of the whole population. We used a validated rating scale to explore ADHD symptoms along separable dimensions to allow a more detailed exploration of the nature of these difficulties among VP children. The 18.3% prevalence of SEN among the term-born controls is remarkably similar to the 18.8% prevalence of SEN in the general population,31 providing assurance that our control sample was representative of the general population in terms of academic and behavioural difficulties. Children with significant disabilities and those attending special schools were excluded, and therefore our findings may underestimate the true prevalence of behaviour problems and SEN in the VP population. Although the classification of SEN differs between education systems, there is cross-cultural consistency in behavioural outcomes across preterm and low birthweight populations.32 Thus, the potential for VP children with inattention to be missed in school is likely to be universal and warrants further investigation.

    Conclusion

    ADHD symptoms in VP children are associated with a core deficit in inattention. Given the constellation of behavioural outcomes following preterm birth, VP children with inattention may not be readily identified as having problems in the classroom. If such problems are undetected these may have a detrimental impact on VP children's learning and attainment at school. Enhancing teachers’ awareness of the behavioural outcomes of this vulnerable population and screening for inattention may be beneficial in identifying VP children with subtle difficulties that may otherwise go undetected.

    Acknowledgments

    The authors thank the children, parents and teachers who took part in the Premature Infants’ Skills in Mathematics (PRISM) study (http://www.prismstudy.org.uk).

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    Supplementary materials

    • Supplementary Data

      This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

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    Footnotes

    • Contributors EB contributed to data entry, analysis and interpretation, drafted the manuscript and approved the submitted version. LC, CG, NM and SJ conceptualised and designed the study, revised the manuscript for intellectual content and approved the submitted version. VS acquired the data, contributed to data analysis and interpretation, revised the manuscript for intellectual content and approved the submitted version.

    • Funding This study was funded by an Action Medical Research project grant to SJ, CG, LC and NM (ref SP4575). NM receives a proportion of funding from the Department of Health's NIHR Biomedical Research Centres funding scheme at UCLH/UCL. CG is funded by a Royal Society Dorothy Hodgkin Fellowship.

    • Competing interests None.

    • Ethics approval Derbyshire National Health Service Research Ethics Committee.

    • Provenance and peer review Not commissioned; externally peer reviewed.

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      Archives of Disease in Childhood 2014; 99 i-i Published Online First: 17 Aug 2014. doi: 10.1136/archdischild-2014-307267